Cranial sexual dimorphism in New World marsupials and a ...

Cranial sexual dimorphism in New World marsupials and a test ofRensch’s rule in Didelphidae

DIEGO ASTUA*

Laboratorio de Mastozoologia, Departamento de Zoologia, Centro de Ciencias Biologicas, Universidade Federal de

Pernambuco, Avenida Professor Moraes Rego, s/n. Cidade Universitaria, 50670-420 Recife, Pernambuco, Brasil

* Correspondent: [email protected]

This study assessed the occurrence of sexual size dimorphism (SSD) and sexual shape dimorphism (SShD) in

the skull and mandible of representatives of most species within the 3 orders of living New World opossums,

Didelphimorphia, Paucituberculata, and Microbiotheria, using geometric morphometrics. Centroid sizes and

partial warps were extracted from landmarks set on images of the dorsal, ventral, and lateral views of the skull

and lateral view of the mandible, and were compared between sexes to estimate SSD and SShD. Specimens

totaling 2,932 from 71 species of Didelphidae, 5 species of Caenolestidae, and 1 species of Microbiotheriidae

were analyzed. SSD was variable in the Didelphimorphia and the Paucituberculata and absent in

Microbiotheria. Similar results were found for SShD, but SSD and SShD are not clearly coupled. I also

evaluated the validity of Rensch’s rule—the widely observed phenomenon of correlated increases in SSD and

body size for male-biased sexual dimorphism, or correlated decreases in SSD in body size for female-biased

sexual dimorphism—in the Didelphidae. Didelphids span 2 orders of magnitude in body size, and, when

present, sexual dimorphism is male-biased. Regressions of SSD and SShD estimators onto size, using

phylogenetic independent contrasts, showed either no significant relationship between SSD or SShD with size

in any of the structures and views analyzed, or a trend contrary to Rensch’s rule (smaller species more

dimorphic, but with male-biased dimorphism). Lack of adherence to Rensch’s rule in Didelphimorphia may

relate to a lack of social interactions and male territoriality, usually associated with such a trend via sexual

selection. If the trend contrary to Rensch’s rule is real, an explanation may lie in the increasing amount of small-

bodied species that recently have been found to be semelparous and thus subject to stronger selection for larger

males. DOI: 10.1644/09-MAMM-A-018.1.

Key words: Caenolestidae, Didelphidae, Microbiotheriidae, Rensch’s rule, sexual shape dimorphism, sexual size

dimorphism

E 2010 American Society of Mammalogists

Living New World opossums are currently classified in 3

orders. Didelphimorphia contains a single family (Didelphi-

dae) and includes 19 genera and .90 species that range in

body size from 10 g (Monodelphis and Hyladelphys) to

.2,000 g (Didelphis). The 2 remaining orders, considerably

less diverse, are probably relict lineages. Living representa-

tives of Paucituberculata include only 3 genera and 6 species

from a single family (Caenolestidae) and are all small-bodied,

weighing from 25 to 50 g. Microbiotheria contains a single

monotypic family (Microbiotheriidae), with a sole, small-

bodied (627 g) species, Dromiciops gliroides.

Sexual dimorphism in qualitative and quantitative charac-

ters in New World opossums has been reported for several

species of Didelphidae (Bergallo and Cerqueira 1994; Maunz

and German 1996; Oliveira et al. 1992; Pine et al. 1985),

Caenolestidae (Bublitz 1987), and Microbiotheriidae (Hersh-

kovitz 1999). However, most morphometric studies that

included quantitative appraisals of sexual dimorphism were

restricted to a single genus (Cerqueira and Lemos 2000;

Lemos and Cerqueira 2002; Ventura et al. 1998), addressed

variation within a single species (Lopez-Fuster et al. 2000,

2002; Pine et al. 1985; Steiner and Catzeflis 2003), or included

only a single representative of each genus analyzed (Astua de

Moraes et al. 2000). Therefore, a comprehensive analysis of

sexual dimorphism in size and shape over a broad taxonomic

range is still lacking for didelphids.

Rensch’s rule states that when males are larger than

females, greater amounts of sexual dimorphism in body size

will be found in larger species. Inversely, greater amounts of

sexual dimorphism are expected in smaller species when

w w w . m a m m a l o g y . o r g

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females are larger than males. Rensch’s rule has been

evaluated in taxa ranging from arthropods to vertebrates

(Abouheif and Fairbairn 1997). The validity of the rule has

been assessed in a wide variety of mammals, but most

analyses lacked statistical tests or did not use phylogenetic

information when performing regressions. Groups of mam-

mals adequately tested for the occurrence of Rensch’s rule

include carnivores, primates, and ungulates (Abouheif and

Fairbairn 1997; Smith and Cheverud 2002), but an appraisal of

Rensch’s rule in marsupials other than kangaroos and

wallabies, which did not include phylogenetic information,

never has been made.

Recently, geometric morphometrics have been used for the

evaluation of sexual dimorphism in a variety of mammal

groups (Cardini and Tongiorgi 2003; Monteiro-Filho et al.

2002; O’Higgins and Collard 2004) because they allow for a

formal separation of size and shape (Zelditch et al. 2004) and

thus independent estimates of size and shape dimorphism

(Franklin et al. 2006; Gidaszewski et al. 2009; Hood 2000).

The purpose of this study was to use geometric morphometric

descriptors to evaluate and quantify the occurrence of sexual

dimorphism in size and shape of the skull and mandible within

the 3 living orders of New World opossums. The data set

obtained here, combined with recent advances in the study of

the phylogenetic relationships of species within the Didelphi-

dae, allowed an evaluation of the application of Rensch’s rule

to this group, assessing the relation of both sexual size and

shape dimorphism to body size.

MATERIALS AND METHODS

Samples.—I used museum specimens and included only

those unambiguously identifiable based on either published

diagnostic characters or geographic distributions. Whenever

possible I included specimens from limited geographic regions

and from a single subspecies. To maximize taxonomic

representation I limited samples of well-represented species

to approximately 30 males and females. For rarer taxa I

examined all available specimens. Specific criteria used for

each species’ sample are detailed in Astua de Moraes (2004).

To avoid ontogenetic variation I used only adult specimens.

Specimens were considered adults when presenting fully

erupted P3, p3, M4, and m4 (Astua and Leiner 2008; Luckett

and Hong 2000; Tribe 1990; Tyndale-Biscoe and Mackenzie

1976). Taxonomy follows Gardner (2007). Rare and more

recently described didelphid genera such as Cryptonanus and

Chacodelphys were not included.

I obtained data for a total of 2,932 specimens from 71

species of Didelphidae, 5 species of Caenolestidae, and 1

species of Microbiotheriidae, for a grand total of 21 genera

and 77 species (Table 1; a complete list of the specimens

examined is available upon request). This represented all

TABLE 1.—Species examined and sample sizes used in this analysis. Sample sizes are presented as ranges of sample sizes for each sex,

because some specimens could not be used in all views due to missing or broken structures that prevented the setting of 1 or more landmarks.

Genus Species and sample sizes (males/females)

Didelphimorphia

Caluromys C. derbianus: 30–36/32–39; C. lanatus: 29–30/27–31; C. philander: 44–52/40–50

Caluromysiops C. irrupta: 3/1–2

Chironectes C. minimus: 30–38/21–25

Didelphis D. albiventris: 29–32/28–31; D. aurita: 28–42/27–35; D. imperfecta: 9/7; D. marsupialis: 26–27/33–35; D. pernigra: 26–27/34–36;

D. virginiana: 3–30/16–31

Gracilinanus G. aceramarcae: 4/3; G. agilis: 30–35/31–33; G. dryas: 5/2–3; G. marica: 6–7/1–2; G. microtarsus: 22–25/7–8

Hyladelphys H. kalinowskii: 3/2

Lestodelphys L. halli: 2/1

Lutreolina L. crassicaudata: 29–32/23–26

Marmosa M. lepida: 2–3/3–4; M. mexicana: 27–29/17–20; M. murina: 27–34/28–30; M. robinsoni: 25–31/30–33; M. rubra: 9–11/5–7; M.

tyleriana: 4–6/2; M. xerophila: 24–28/32–33

Marmosops M. fuscatus: 20–22/9–10; M. impavidus: 32–34/17–23; M. incanus: 31–34/30–31; M. invictus: 3/5; M. noctivagus: 27–31/34–38; M.

ocellatus: 9–12/4–5; M. parvidens: 8–10/6–7; M. paulensis: 15–17/15–17; M. pinheiroi: 10–11/6–9

Metachirus M. nudicaudatus: 28–33/24–27

Micoureus M. alstoni: 3–4/4–4; M. constantiae: 10–11/6–8; M. demerarae: 28–33/24–26; M. paraguayanus: 23–28/23–26; M. phaeus: 6–7/6–8;

M. regina: 26–33/34–37

Monodelphis M. adusta: 8–10/3–4; M. americana: 7–12/12–15; M. brevicaudata: 23–28/25–27; M. dimidiata: 2–5/1–4; M. domestica: 28–33/27–

32; M. glirina: 27–31/29–33; M. palliolata: 1/7; M. sorex: 2/2

Philander P. andersoni: 16–21/15–18; P. frenatus: 29–33/30–32; P. mcilhennyi: 8–9/4–5; P. opossum: 26–31/23–27

Thylamys T. cinderella: 6–7/1; T. elegans: 25–26/20–22; T. karimii: 8/8; T. pallidior: 34–40/22–25; T. pusillus: 7–8/3–6; T. sponsorius: 10–12/

5–8; T. tatei: 4/4–6; T. venustus: 2/1

Tlacuatzin T. canescens: 25–29/18–20

Paucituberculata

Caenolestes C. caniventer: 3/10–12; C. convelatus: 5/8–10; C. fuliginosus: 49–57/36–38

Lestoros L. inca: 38–43/32–34

Rhyncholestes R. raphanurus: 8–10/14–15

Microbiotheria

Dromiciops D. gliroides: 19–23/12–18

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recognized species for most genera. Adequate samples for

sexual dimorphism analyses were unavailable for several

species, and only specimens with �3 males and females were

included in statistical comparisons. Data for species with

smaller sample sizes are presented only to provide qualitative

comparisons; these include rare taxa such as Hyladelphys,

Lestodelphys, and Caluromysiops.

Images and landmarks.—I took digital images of the skull

(in dorsal, ventral, and lateral view) and the mandible with a

Nikon Coolpix 995 camera (Nikon, Inc., Melville, New York)

at a resolution of 1,280 3 960 pixels. Skulls and mandibles

always were oriented similarly; that is, frontal plane passing

through the root of incisors and base of occipital condyle (for

dorsal views), palate plane (for ventral views), midsagittal

plane (for lateral views), and the plane including coronoid

process and horizontal ramus (for the mandible), always

parallel to the lens plane. All images included a ruler for scale.

For some species I also used images taken for a previous study

(Astua de Moraes et al. 2000).

I determined 12 landmarks for the dorsal view of the skull, 14

for the ventral view, 19 for the lateral view, and 19 for the

lateral view of the mandible (Fig. 1). Landmarks were digitized

using TPSDig (Rohlf 2006). For the dorsal and ventral view of

the skull I set landmarks on both the left and right and averaged

coordinates from both sides using the midline as reflection axis.

This controlled for variation due to skull asymmetry and

resulted in using coordinates representing 1 side of the skull in

the analyses. When only a specific landmark was missing on 1

side of the skull, I used the coordinates from the opposite side

instead of the average coordinates.

I tested all landmarks for repeatability. For each view 30

specimens from 1 species were selected randomly, and all

landmarks were digitized twice, randomly reordering the

specimens between the 2 sampling events. I estimated repeat-

ability as the intraclass correlation coefficient, which was

derived from an analysis of variance on the x and y coordinates

of each landmark using individuals as the factor. This took into

account intraclass variability (error in locating landmark

position) and interclass variation (real differences between

individuals—Falconer 1989). Repeated measurements of the x

and y coordinates of all landmarks exhibited ,10% error, and

the error rate was ,5% in 95% of the cases. All landmarks were

considered satisfactory and included in subsequent analyses.

Statistical analyses.—Landmark configurations were sub-

mitted to a generalized Procrustes alignment (Rohlf and Slice

1990) to remove effects of position, orientation, and isometric

size in landmark configurations, thus formally separating size

and shape. The size variable used in generalized Procrustes

alignment was centroid size, the square root of the sum of

squared distances between each landmark and the centroid of

the whole landmark configuration. This procedure reduces

size to a single univariate measure that incorporates the

multivariate nature of size and was therefore used for

evaluation of sexual size dimorphism (SSD). The remaining

landmark configurations retained only shape information and

were used for evaluation of sexual shape dimorphism (SShD).

I evaluated SSD using centroid sizes for each view. To test

for existence of SSD in each species I compared centroid sizes

between males and females using t-tests (Zar 1996) whenever

allowed by sample sizes. Because 4 tests for each species were

performed, a Bonferroni correction within each species was

applied, thus yielding a P-value of 0.0125. I evaluated SShD

using the complete set of partial warps, including uniform

components, as shape variables. To assess the existence of

SShD in each species I compared male and female shapes

using Goodall F-tests whenever allowed by sample sizes. To

confirm these results, especially for species with reduced

sample sizes, species that presented significant SShD were

FIG. 1.—Landmarks used in the analyses presented on skulls of A,

B) Marmosa robinsoni (A: dorsal view, B: ventral view) and C)

Didelphis albiventris (lateral view) and D) mandible of Lutreolina

crassicaudata. Bars 5 1 cm.

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submitted to a resampling Goodall F-test with 2,500

repetitions. Goodall F-tests and resampling F-tests were

performed with the Two-Groups module of the IMP suite

(Sheets 2004). Mean Procrustes distances between sexes for

each species also were calculated to visualize the amount of

SShD.

Size and shape sexual dimorphism and Rensch’s rule

in Didelphidae.—To assess the existence of Rensch’s rule in

the Didelphidae I regressed the natural logarithm of the ratio

between centroid sizes of males and females (SSD estimators)

onto the natural logarithm of female centroid size (Smith

1999; Smith and Cheverud 2002). An absence of correlation

between SSD and size would result in a slope that did not

differ significantly from 0. Regressions used a least-squares

fit, because this reflects the distribution of error when the

dependent variable is a ratio but the independent variable is a

direct measurement (Smith 1999).

Traditional analyses of Rensch’s rule usually assess the

existence of increasing SSD with increasing body size, but

with a few exceptions (Drovetski et al. 2006), most analytical

approaches do not consider differences in shape between

sexes. I assessed the relation between SShD and body size to

determine whether shape differences increased with increasing

body size (hereafter termed ‘‘Rensch’s rule for shape’’ to

avoid confusion). SShD was estimated based on the mean

tangent distance between sexes. Tangent distances are

obtained by projecting Procrustes distance between sexes

(which represent the distance between any 2 shapes in

Kendall’s shape space, thus, in this case, the difference in

shape between sexes) onto a plane tangent to Kendall’s

multidimensional curved shape space. Because Procrustes

distances actually lie in the curved shape space, they are not

suitable for use in standard statistical procedures that assume

Euclidean linear distances. The correspondence between

Procrustes distances and tangent distances can be estimated

by correlating these 2 distances for each pair of specimens in

the analyses. All analyses yielded a correlation coefficient of

1, demonstrating that tangent distances were good proxies for

Procrustes distances. I then regressed tangent distances onto

the natural logarithm of female centroid size (the same

indicator of size used for SSD) to test for the relation between

SShD and body size. As for SSD, the absence of a relationship

would yield a slope that does not differ significantly from 0

(i.e., shape difference does not change with body size).

Phylogenies.—Because these data are not statistically

independent due to phylogenetic relationships among species,

it was necessary to conduct statistical analyses within a

phylogenetic framework (Harvey and Pagel 1991; Martins and

Hansen 1997). I used phylogenetic independent contrasts to

account for relationships between the studied taxa (Felsenstein

1985).

Although recent studies have increased the number of taxa

used in phylogenetic analyses of Didelphidae (Jansa and Voss

2005; Voss and Jansa 2003, 2009; Voss et al. 2004, 2005),

they do not encompass all of the taxa available for this study

(.60 species). Therefore, I manually assembled a larger tree

to include all taxa for which I had SSD or SShD data. I

rearranged the original supertree of Cardillo et al. (2004) to

match the topology of Voss and Jansa (2009) for relationships

at the generic level. This assumes monophyletic genera which,

based on current knowledge, is probably reasonable for most

taxa except Marmosa (Voss and Jansa 2009). However, the

clade Marmosa + Micoureus (after exclusion of Tlacuatzin)

was retained because it has been recovered as monophyletic in

most analyses, including the supertree (Cardillo et al. 2004)

and all molecular and morphological analyses (Voss and Jansa

2009).

Phylogenetic independent contrasts were calculated with the

PDAP:PDTREE module (Midford et al. 2008) of Mesquite

(Maddison and Maddison 2008). All analyses were repeated

for the 3 views of the skull and the mandible. Because this

phylogeny lacked branch lengths, I evaluated 2 methods of

assigning arbitrary branch lengths: all branch lengths equal to

1, and the branch length estimation method proposed by Pagel

(1992), as implemented in Mesquite. Of the 2, only the method

proposed by Pagel (1992) did not violate the assumptions of

independence of absolute values of standardized contrasts and

their standard deviations. Even with this method, some views

were excluded from the analyses for violating such assump-

tion.

The tree included polytomies (Fig. 2), reflecting phyloge-

netic uncertainty in some nodes. Therefore, I used the bounded

degrees of freedom approach suggested by Purvis and Garland

(1993), because previous tests of this approach have shown

that independent contrasts can be used even in the presence of

such phylogenetic uncertainty (Garland and Diaz-Uriarte

1999). The method involves calculating upper and lower

limits for the degrees of freedom used to determine the

significance of the regression. All polytomies were converted

to a series of bifurcations of length 0, and thus m 2 1 contrasts

are computed in each polytomy with m branches. However,

because we cannot know whether multifurcating nodes

represent soft or hard polytomies (representing an unknown

phylogeny or a true simultaneous speciation event, respec-

tively), the calculated degrees of freedom are bounded. The

upper bound is calculated assuming that all multifurcations are

hard polytomies, and the corresponding degrees of freedom

are n 2 2 (where n is the number of terminal taxa and n 2 1 is

the number of contrasts). The lower bound is calculated

assuming that all polytomies are soft polytomies, and is

calculated as p 2 1 (where p is the number of real bifurcating

nodes). Regressions then are repeated using upper and lower

bounds to determine how this affects results.

RESULTS

Sexual size and shape dimorphism.—Size comparisons

between sexes for all species with adequate sample sizes are

presented in Table 2. With the exception of Tlacuatzin and the

rare genera with small samples (Hyladelphys and Lestodel-

phys), all remaining genera of Didelphidae and Caenolestidae

contained some species with SSD, at least in 1 of the views. D.


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gliroides did not exhibit significant SSD in the skull or the

mandible. Shape comparisons between sexes for all species

with adequate sample sizes are presented in Table 3. All

genera presented some species with SShD, at least in 1 of the

views.

Allometric relation between SSD or SShD and size in

Didelphidae.—The relationship between SSD or SShD and

size was evaluated for the skull in dorsal and ventral views

and the mandible. Regressions based on the dorsal view of the

skull and the mandible were not significant, but a significant

FIG. 2.—Tree used to produce the phylogenetic independent contrasts used in regressions of sexual size dimorphism (SSD) and sexual shape

dimorphism (SShD) on size. Refer to text for additional details.


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TABLE 2.—Sexual size dimorphism in New World opossums. For each view of the skull and the mandible, mean centroid size and standard

deviation (CS 6 SD), and significance of t-tests (boldface type: P , 0.0125, after Bonferroni correction) between male and female centroid sizes

are indicated.

Skull (dorsal) Skull (ventral) Skull (lateral) Mandible

== RR == RR == RR == RR

Didelphimorphia

Caluromys derbianus 68.4 6 3.4 68.1 6 2.9 72.8 6 3.8 72.2 6 3.5 88.7 6 4.5 87.5 6 4.2 70.5 6 4.3 69.0 6 3.3

C. lanatus 72.2 6 2.4 71.0 6 2.8 76.2 6 2.6 75.3 6 3.4 93.1 6 3.1 91.8 6 4.3 73.2 6 2.9 71.6 6 2.9

C. philander 63.2 6 3.7 61.9 6 4.0 66.5 6 4.5 64.0 6 4.6 81.0 ± 5.2 78.0 ± 5.8 63.9 6 4 62.2 6 4.5

Caluromysiops irrupta 76.5 6 0.9 74.0 6 0.3 80.6 6 1.4 77.9 6 0.4 97.0 6 1.1 94.0 6 0.2 75.5 6 2.3a 73.2 6

Chironectes minimus 85.8 6 3.9 83.9 6 4.1 93.4 6 4.5 92.0 6 4.4 113.9 6 5.8 110.7 6 6.2 94.9 6 4.3 92.9 6 4.6

Didelphis albiventris 105.5 ± 8.0 97.8 ± 7.5 116.0 ± 8.7 107.0 ± 8.1 137.4 ± 10.7 126.3 ± 10.1 115.0 ± 6.9 107.7 ± 8.4

D. aurita 122.6 ± 12.0 108.6 ± 7.5 132.9 ± 12.9 119.2 ± 7.9 160.5 ± 15.7 143.0 ± 10.5 133.3 ± 11.6 123.1 ± 7.3

D. imperfecta 101.5 6 9.4 99.5 6 10.3 111.7 6 11.5 109.6 6 11.1 132.6 6 12.2 129.5 6 14.2 109.6 6 10.5 108.6 6 11.4

D. marsupialis 123.3 6 6.0 120.1 6 6.8 136.5 6 6.4 133.4 6 7.4 163.3 6 8.7 158.9 6 10.0 135.0 6 5.4 133.2 6 7.1

D. pernigra 117.1 6 9.1 112.4 6 7.3 129.6 6 9.8 126.2 6 8.6 153.7 6 11.9 149.1 6 10.6 128.3 6 9.3 124.8 6 8.5

D. virginiana 138.3 ± 8.7 127.7 ± 9.2 156.7 ± 10.7 144.0 ± 12.2 188.0 ± 13.3 171.8 ± 15.6 155.0 6 3.5 146.0 6 14.0

Gracilinanus aceramarcae 33.5 6 0.7 31.8 6 0.7 34.0 6 0.6 32.7 6 0.8 42.1 6 1.3 40.1 6 1.4 32.2 6 0.5 30.5 6 0.8

G. agilis 33.0 ± 1.3 31.4 ± 1.4 34.8 ± 1.8 32.9 ± 1.8 42.0 ± 2.1 40.2 ± 2.1 33.1 ± 1.5 31.5 ± 1.7

G. dryas 32.0 6 1.2 31.8 6 0.2 3 6 1.5 32.6 6 0.6 40.3 6 1.8 40.2 6 0.5 30.0 6 1.2 30.6 6 0.5

G. marica 32.2 6 1.1a 29.1 31.5 6 1.4 29.8 6 1.2

G. microtarsus 34.4 ± 1.7 32.3 ± 1.6 36.2 ± 2.4 33.6 ± 2.0 44.0 ± 2.8 40.9 ± 2.7 34.7 ± 2.0 32.1 ± 2.1

Hyladelphys kalinowskii 25.7a 26.0 6 0.4 26.2 6 0.3 26.7 6 0.6

Lestodelphys halli 41.9 6 0.8a 36.4 45.1 6 0.9a 39.3 54.7 6 0.9a 47.0 44.0 6 1.2a 37.2

Lutreolina crassicaudata 79.5 ± 5.8 70.7 ± 5.8 89.4 ± 7.0 79.1 ± 6.8 104.0 ± 8.2 91.7 ± 7.6 85.9 ± 6.5 76.9 ± 6.3

Marmosa lepida 33.1 6 0.9 33.0 6 1.3 33.2 6 0.6 33.1 6 1.9 41.5 6 0.4 41.3 6 1.8 31.4 6 0.3 31.8 6 1.0

M. mexicana 39.7 ± 2.5 37.2 ± 1.5 42.0 ± 3.1 38.7 ± 1.9 51.0 ± 3.7 47.0 ± 2.0 39.0 ± 3.0 36.6 ± 1.5

M. murina 42.1 ± 2.2 39.9 ± 1.8 44.9 ± 2.7 41.0 ± 2.3 54.5 ± 3.5 51.0 ± 2.8 41.9 ± 2.2 40.0 ± 2.2

M. robinsoni 47.5 ± 2.5 44.1 ± 1.7 50.0 ± 2.8 46.2 ± 2.1 61.7 ± 3.2 56.7 ± 2.5 47.6 ± 2.7 44.0 ± 2.1

M. rubra 43.7 6 1.3 42.3 6 1.1 46.3 6 1.0 45.0 6 1.9 55.8 6 1.5 55.3 6 2.5 44.6 6 1.3 43.7 6 1.3

M. tyleriana 37.8 6 0.7 41.1 6 6.6 40.0 6 1.2 44.1 6 9.0 48.9 6 1.2 53.2 6 10.1 38.1 6 0.8 41.7 6 6.5

M. xerophila 38.9 ± 2.0 36.5 ± 1.3 41.7 ± 2.2 38.8 ± 1.5 50.1 ± 2.6 46.8 ± 1.9 40.3 ± 2.2 37.5 ± 1.5

Marmosops fuscatus 42.8 ± 2.7 38.9 ± 1.9 45.6 ± 3.0 41.2 ± 2.1 55.0 ± 3.9 49.3 ± 2.5 43.6 ± 2.9 40.0 ± 2.1

M. impavidus 40.1 ± 2.4 38.1 ± 1.8 42.6 ± 2.8 39.8 ± 2.2 51.2 ± 3.4 48.0 ± 2.9 39.6 ± 2.5 37.6 ± 2.3

M. incanus 45.6 ± 2.8 41.8 ± 2.3 48.9 ± 3.7 44.6 ± 2.7 59.0 ± 4.5 53.5 ± 3.2 46.7 ± 3.4 42.3 ± 2.8

M. invictus 35.2 6 0.2 34.4 6 0.7 36.8 6 0.6 36.0 6 0.9 44.2 6 0.3 43.4 6 0.8 35.0 6 0.5 34.0 6 0.7

M. noctivagus 44.5 ± 2.3 42.3 ± 2.1 47.6 ± 3.1 45.1 ± 2.3 57.5 ± 3.7 54.4 ± 2.7 44.5 ± 2.7 42.6 ± 2.5

M. ocellatus 39.6 6 1.0 37.4 6 2.0 42.5 ± 1.8 38.9 ± 2.3 51.1 6 2.5 47.0 6 3.1 39.6 ± 1.9 36.9 ± 1.8

M. parvidens 33.7 6 0.9 33.2 6 1.9 34.6 6 1.1 34.5 6 2.1 41.8 6 1.5 41.0 6 2.5 33.0 6 0.9 33.1 6 1.6

M. paulensis 42.1 ± 2.1 39.8 ± 2.4 45.1 ± 2.6 42.5 ± 2.6 54.3 ± 2.9 51.1 ± 3.3 42.8 ± 1.8 40.5 ± 2.5

M. pinheiroi 34.4 ± 0.7 33.2 ± 1.0 35.9 ± 0.8 34.1 ± 0.5 43.3 ± 1.2 41.7 ± 1.2 33.9 6 1.0 33.0 6 0.8

Metachirus nudicaudatus 68.5 6 2.9 63.8 6 2.5 71.6 6 3.8 70.2 6 3.5 85.2 6 4.1 83.8 6 3.4 74.1 ± 3.5 71.6 ± 2.6

Micoureus alstoni 52.5 6 1.3 50.5 6 1.9 55.7 6 1.5 58.6 6 8.7 68.7 6 1.9 65.6 6 2.6 53.0 6 1.7 51.9 6 1.8

M. constantiae 48.3 6 3.6 46.0 6 1.8 51.5 6 3.8 49.5 6 1.9 62.7 6 5.0 59.0 6 2.4 50.2 6 3.9 47.1 6 1.9

M. demerarae 51.9 ± 2.5 49.2 ± 2.5 55.2 ± 2.6 52.4 ± 3.0 67.4 ± 3.0 63.6 ± 3.7 53.6 6 2.3 52.0 6 2.8

M. paraguayanus 51.3 6 2.4 50.4 6 2.8 54.9 6 3.2 54.0 6 3.5 67.0 6 4.0 65.1 6 4.3 53.7 6 2.7 52.8 6 3.7

M. phaeus 45.3 6 1.4 44.7 6 2.1 47.9 6 1.7 46.9 6 2.3 58.9 6 2.3 57.5 6 3.5 45.5 6 1.7 44.6 6 1.1

M. regina 52.4 ± 2.4 50.1 ± 2.6 56.1 ± 3.4 53.4 ± 3.1 68.9 ± 3.7 65.4 ± 3.8 53.7 ± 3.6 51.6 ± 3.0

Monodelphis adusta 31.2 6 2.2 29.4 6 1.4 35.0 6 2.6 33.1 6 1.2 41.2 6 2.9 38.5 6 2.0 32.2 6 2.3 30.6 6 1.3

M. americana 32.9 6 3.7 32.0 6 1.7 36.0 6 4.6 35.1 6 2.2 43.0 6 5.4 41.1 6 2.4 35.4 6 3.3 33.5 6 2.3

M. brevicaudata 44.1 ± 3.1 40.2 ± 2.1 48.9 ± 3.6 44.6 ± 2.3 57.8 ± 4.2 52.0 ± 2.7 46.0 ± 3.3 42.1 ± 2.1

M. dimidiata 32.4 6 4.3a 26.7 39.3 6 8.7a 29.8 35.8 6 9.1 31.1 6 5.3

M. domestica 46.0 6 3.9 44.3 6 2.3 51.8 ± 4.1 49.0 ± 2.8 60.3 6 4.8 57.5 6 3.3 48.8 ± 3.5 46.8 ± 2.6

M. glirina 46.5 ± 2.7 41.8 ± 1.7 52.2 ± 3.2 47.0 ± 2 61.5 ± 3.5 54.9 ± 2.5 48.7 ± 2.9 44.1 ± 1.9

M. palliolata 44.0 6 2.4a 42.5

M. sorex 31.6 6 0.7 29.2 6 4.3 35.5 6 1.1 32.6 6 6.0 41.9 6 1.3 38.7 6 6.4 32.1 6 0.3 30.1 6 5.1

Philander andersoni 84.6 ± 3.7 79.4 ± 3.3 94.1 ± 4.6 88.1 ± 3.7 111.9 ± 5.5 104.8 ± 4.2 92.3 ± 3.6 86.7 ± 4.0

P. frenatus 77.0 ± 6.4 69.7 ± 4.2 84.3 ± 7.0 75.8 ± 4.2 100.8 ± 8.3 90.6 ± 5 85.5 ± 7.0 78.2 ± 4.0

P. mcilhennyi 86.7 6 4.2 82.8 6 4.8 97.2 6 4 92.3 6 5.9 115.0 6 5.2 109.0 6 7.2 94.6 6 4.9 91.0 6 5.3

P. opossum 84.2 6 5.1 82.9 6 4.6 93.9 6 6.2 92.6 6 5.9 111.1 6 7.6 108.4 6 7.0 92.6 6 4.7 90.9 6 5.1

Thylamys cinderella 34.6 6 2.2a 35.7 36.6 6 2.5a 37.9 44.0 6 3.5 46.0 35.1 6 2.5 35.4

T. elegans 34.3 6 1.5 33.4 6 1.6 36.6 6 1.9 35.6 6 2.2 44.1 6 2.1 42.7 6 2.5 34.1 6 1.8 33.0 6 1.7

T. karimii 35.3 6 1.4 33.5 6 1.5 38.0 6 1.6 35.7 6 2.1 46.2 ± 1.8 43.1 ± 2.4 35.7 6 1.3 33.6 6 1.9

T. pallidior 31.8 6 1.6 30.9 6 1.3 33.8 6 1.8 32.8 6 1.5 40.5 6 2.2 39.0 6 1.6 31.0 6 1.7 30.6 6 1.4

T. pusillus 30.8 6 1.0 29.7 6 1.6 32.4 6 1.1 31.1 6 2.0 39.2 6 1.6 38.6 6 1.6 32.7 6 2.9 30.1 6 1.5


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negative slope was found for the analysis of the ventral view

of the skull (Fig. 3A). Results for SShD are similar to those for

SSD, with significant negative slopes found for the skull in

both views (Figs. 3B and 3C) and no relationship between

SShD and size in the mandible.

DISCUSSION

Significant sexual dimorphism in size, shape, or both was

found in Didelphimorphia and Paucituberculata, with signif-

icantly dimorphic species being found in almost all genera.

The only living representative of Microbiotheria is not

sexually dimorphic. In the Didelphidae 50–60% of the species

present significant sexual dimorphism in cranial size or shape,

and in all cases males are larger than females. If these species

follow Rensch’s rule, the larger species should be more

dimorphic. However, didelphids do not seem to follow this

pattern, because slopes either did not differ significantly from

0 (indicating that in these cases the amount of SSD or SShD is

uncorrelated to size) or were negative (indicating that smaller

species were more dimorphic, even though males were larger

than females). Possible explanations for the lack of adherence

to Rensch’s rule may include the lack of rigid social systems

or a possible prevalence of reproductive strategies leading to

greater SSD or SShD in smaller species.

Most previous analyses of sexual dimorphism as it relates to

Rensch’s rule refer to body size dimorphism. I used cranial

size as a proxy for body size when comparing these results

with previous estimates, because cranial size can be expected

to vary accordingly to body size. A correlation between mean

body weight (Smith et al. 2003) and mean cranial size

(centroid size, from this study) for 46 didelphid species

showed a correlation of r 5 0.91, thus allowing for a

comparison between these and previous results.

Sexual dimorphism in Didelphidae.—The only woolly

opossum with data on sexual dimorphism was Caluromys

philander. Presence of SSD in C. philander was detected in

a large sample from French Guiana and in specimens from

a broader geographic area (Astua de Moraes et al. 2000;

Richard-Hansen et al. 1999), but SSD varied across localities

(Caramaschi 2005). Significant SSD was confirmed here for

C. philander only (skull and mandible), yet significant SShD

was found in Caluromys derbianus and C. philander in at least

1 view each (Table 3).

Opossums of the genus Didelphis are some of the best-

studied didelphid species, although existing assessments of

their sexual dimorphism are contradictory. I found SShD for

all 6 currently recognized species (Table 3), but only D.

virginiana, D. aurita, and D. albiventris presented significant

SSD (Table 2). The significant SSD found here in D. aurita,

D. albiventris, and D. virginiana and SShD in D. virginiana

were reported in other studies (Cerqueira and Lemos 2000;

Gardner 1973; Lemos and Cerqueira 2002). This study also

corroborates previous evidence for a lack of SSD in D.

imperfecta, D. pernigra, and D. marsupialis (Ventura et al.

2002). The latter species, however, also has been reported to

exhibit SSD (Cerqueira and Lemos 2000; Richard-Hansen et

al. 1999; Tyndale-Biscoe and Mackenzie 1976).

The remaining genera of large-bodied opossums showed

different levels of SSD and SShD. Although Lutreolina

crassicaudata proved to be highly dimorphic in size, SSD

was absent in Chironectes minimus and found only in the

mandible in Metachirus nudicaudatus (Table 3). Two species

of Philander (P. andersoni and P. frenatus) were highly

dimorphic in size, and 2 (P. mcilhennyi and P. opossum) were

not. Results for SShD were similar, with half the species being

dimorphic. L. crassicaudata has been reported as a highly

dimorphic species (Graipel et al. 1996; Lemos et al. 2001), but

contrary to previous studies (Lemos et al. 2001; Richard-

Hansen et al. 1999) I found no SSD in C. minimus and M.

nudicaudatus. As in Didelphis, contradictory evidence exists

for SSD in M. nudicaudatus (Patton et al. 2000; Richard-

Hansen et al. 1999). These contrasting results are indicative of

significant morphological variation in a widely geographically

distributed taxon that possibly is represented by several

species, as suggested by ongoing studies (Silva 2005; Vieira

2006). Dimorphism in P. frenatus had already been reported in

a previous analysis (Astua de Moraes et al. 2000), but the lack

TABLE 2.—Continued.

Skull (dorsal) Skull (ventral) Skull (lateral) Mandible

== RR == RR == RR == RR

T. sponsorius 35.0 6 1.7 36.2 6 1.4 37.2 6 2.1 38.8 6 1.9 44.9 6 2.5 46.5 6 2.6 34.6 6 2.0 35.6 6 2.7

T. tatei 35.8 6 1.0 34.4 6 1.4 38.2 6 1.1 37.5 6 1.9 45.8 6 1.1 44.8 6 2.5 35.4 6 1.1 34.0 6 2.1

T. venustus 33.5 6 0.8a 33.4 35.3 6 1.1a 36.9 42.6 6 1.3 44.0 32.9 6 1.4a 34.3

Tlacuatzin canescens 35.7 6 2.0 35.4 6 2.7 37.2 6 3.0 37.0 6 3.1 45.6 6 3.6 45.0 6 3.6 35.9 6 2.0 35.7 6 3.2

Paucituberculata

Caenolestes caniventer 37.8 6 2.9 35.6 6 1.2 40.1 6 2.9 37.9 6 1.6 47.1 6 3.1 44.6 6 1.6 33.1 6 2.1 30.8 6 1.0

C. convelatus 39.1 6 2.1 37.1 6 0.9 42.0 ± 2.6 39.4 ± 1.0 49.3 6 3.2 46.5 6 1.1 33.0 6 2.1 32.0 6 0.6

C. fuliginosus 35.9 ± 1.9 33.9 ± 1.3 37.8 ± 2.3 35.4 ± 1.5 44.3 ± 2.4 41.7 ± 1.7 30.2 ± 1.6 28.7 ± 1.3

Lestoros inca 34.0 ± 1.0 32.7 ± 0.7 35.5 ± 1.1 34.2 ± 1.0 41.9 ± 1.4 40.4 ± 1.1 28.5 ± 0.9 27.5 ± 0.9

Rhyncholestes raphanurus 36.5 6 1.1 35.6 6 0.7 39.0 6 2.0 38.5 6 1.2 44.9 6 1.8 44.0 6 1.3 30.7 6 1.4 29.9 6 1.0

Microbiotheria

Dromiciops gliroides 31.7 6 0.9 32.2 6 0.8 33.5 6 1.1 3 6 1.0 39.6 6 1.1 40.3 6 1.0 29.7 6 1.0 30.0 6 1.0

a Species (or views) were not tested and are presented for qualitative comparison purposes only.


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of SSD found in P. opossum contradicts previous reports

(Lemos et al. 2001; Richard-Hansen et al. 1999).

Most Micoureus species were not dimorphic in size, except

for M. demerarae and M. regina. Micoureus paraguayanus

and M. demerarae recently have been diagnosed as separate

species (Patton and Costa 2003; Patton et al. 2000). Further

differences between these 2 species were observed here,

because only the former presented SSD and SShD in the skull

(Patton et al. 2000). With the exception of Patton et al. (2000),

estimates of sexual dimorphism in Micoureus were unknown

prior to this study.

In Marmosa the presence of SSD in M. murina, M.

xerophila, M. robinsoni, and M. mexicana confirm several

previous reports, although some of these consisted only of

measurement ranges with no statistical tests (Alonso-Mejıa

and Medellın 1992; Lopez-Fuster et al. 2000, 2002; O’Connell

1983; Rossi 2005). The 3 other species of the genus (M.

lepida, M. rubra, and M. tyleriana) are rare in mammal

collections and thus had much smaller sample sizes, which

could have contributed to the absence of SSD. Based on

similarly limited samples, Rossi (2005) also observed low

levels of SSD in these 3 species.

Marmosops was highly dimorphic in size, with most species

showing significant SSD (Table 2). Dimorphism was reported

previously in qualitative characters for the genus (Lunde and

Schutt 1999; Voss and Jansa 2003; Voss et al. 2001). In this

study only M. invictus and M. parvidens did not present

significant SSD, as previously reported for the latter (Pine

1981). This is a problematic species of Marmosops, because

morphological and molecular analyses have suggested that it

contains multiple species (Patton and Costa 2003; Voss and

Jansa 2003; Voss et al. 2001). Estimates of dimorphism may

need to be reevaluated after elucidation of its proper

taxonomic status. Semelparity or partial semelparity have

been proposed for Marmosops incanus and M. paulensis,

based on age classes of museum specimens and field studies

(Leiner et al. 2008; Lorini et al. 1994). Either reproductive

strategy would be consistent with significant dimorphism.

TABLE 3.—Sexual shape dimorphism in New World opossums. For

each view of the skull and mandible mean Procrustes distances

between sexes and results for Goodall F-tests are indicated (boldface

type: significant differences found in Goodall F-tests after

resamplings, using P , 0.0125 for Bonferroni correction).

Mean Procrustes distances:

== 2 RR (31022)

Skull

MandibleDorsal Ventral Lateral

Didelphimorphia

Caluromys derbianus 1.26 0.51 1.46 1.13

C. lanatus 0.85 0.78 1.32 1.18

C. philander 0.70 0.79 1.07 0.91

Caluromysiops irrupta 3.44 2.59 3.90 —

Chironectes minimus 1.43 1.00 1.57 1.79

Didelphis albiventris 2.64 2.77 2.58 2.67

D. aurita 2.56 3.72 3.41 3.75

D. imperfecta 2.29 2.93 3.44 3.42

D. marsupialis 1.43 1.30 1.67 1.13

D. pernigra 1.48 1.41 1.37 1.74

D. virginiana 2.12 1.91 2.31 3.53

Gracilinanus aceramarcae 2.84 1.62 2.62 2.38

G. agilis 1.43 1.49 1.44 1.52

G. dryas 1.27 1.32 1.61 1.96

G. marica — — — 1.99

G. microtarsus 1.42 1.91 2.27 1.83

Lutreolina crassicaudata 2.03 1.79 1.84 2.08

Marmosa lepida 2.91 3.06 2.70 1.94

M. mexicana 1.79 0.96 1.76 1.69

M. murina 1.07 1.56 1.47 1.40

M. robinsoni 1.67 1.71 2.02 2.35

M. rubra 1.69 1.17 1.31 1.10

M. tyleriana 3.15 2.39 3.54 2.79

M. xerophila 1.55 1.16 1.59 1.63

Marmosops fuscatus 2.70 2.21 2.81 2.68

M. impavidus 1.38 1.76 1.93 1.57

M. incanus 1.91 1.42 2.25 1.84

M. invictus 1.65 1.30 1.80 1.33

M. noctivagus 0.99 1.22 1.35 1.38

M. ocellatus 1.81 1.60 1.21 1.90

M. parvidens 2.88 1.47 1.79 1.71

M. paulensis 1.03 1.07 1.30 1.25

M. pinheiroi 1.63 2.03 1.81 2.09

Metachirus nudicaudatus 1.30 1.12 1.35 1.90

Micoureus alstoni 2.09 1.64 2.18 1.79

M. constantiae 1.99 0.96 1.91 2.06

M. demerarae 1.17 1.02 1.29 1.35

M. paraguayanus 0.67 0.72 0.75 1.51

M. phaeus 2.31 0.92 2.50 1.23

M. regina 1.24 1.59 1.55 1.82

Monodelphis adusta 4.02 2.38 2.22 1.99

M. americana 1.26 1.75 2.27 2.42

M. brevicaudata 1.44 1.99 1.95 2.55

M. dimidiata — — — 3.87

M. domestica 0.99 1.09 1.14 1.31

M. glirina 2.34 2.32 2.43 3.05

M. sorex 2.59 3.47 3.31 2.98

Philander andersoni 1.28 1.12 1.41 1.77

P. frenatus 1.64 2.06 2.54 2.68

P. mcilhennyi 2.27 1.15 2.17 1.87

P. opossum 1.72 0.80 1.19 1.34

Thylamys elegans 1.70 0.59 0.93 0.94

T. karimii 1.59 1.12 1.80 2.17

T. pallidior 1.39 0.73 0.90 0.84

TABLE 3.—Continued.

Mean Procrustes distances:

== 2 RR (31022)

Skull

MandibleDorsal Ventral Lateral

T. pusillus 2.82 1.22 2.40 3.08

T. sponsorius 1.40 1.87 2.33 1.41

T. tatei 2.45 1.02 2.03 1.81

Tlacuatzin canescens 1.31 1.09 1.84 1.73

Paucituberculata

Caenolestes caniventer 1.92 2.02 2.55 1.95

C. convelatus 1.79 2.45 2.87 3.26

C. fuliginosus 1.62 1.22 1.99 1.41

Lestoros inca 1.01 0.74 1.30 0.71

Rhyncholestes raphanurus 1.62 0.83 1.36 1.43

Microbiotheria

Dromiciops gliroides 1.39 0.71 1.14 1.13


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Two species of Gracilinanus, G. microtarsus and G. agilis,

exhibited SSD, and SShD was found for the latter (Tables 2

and 3). Costa et al. (2003) also found high levels of sexual

dimorphism in G. agilis, but only a few measurements were

dimorphic for G. microtarsus. In contrast, my results indicate

that both species present similar levels of size and shape

dimorphism. Martins et al. (2006b) reported significant

differences in the diets of males of females of G. microtarsus

and related these differences to reproductive data to suggest

partial semelparity (Martins et al. 2006a). This could explain

the high levels of SSD and SShD found here, because the

specimens referred to as G. microtarsus by Martins et al.

(2006a) are probably G. agilis (S. Loss, Universidade Federal

do Espirito Santo, pers. comm.).

The genus Thylamys has been studied and rearranged in the

last decade and currently includes 10 species (Gardner 2007). I

obtained representatives of 8 of these, with very variable

sample sizes (Table 1). Of those tested, only Thylamys karimii

presented significant SSD, and only in 1 view. This is in

agreement with previous studies of T. karimii, T. pallidior, and

T. elegans (Carmignotto and Monfort 2006; Solari 2003).

The genus Monodelphis, which includes all short-tailed

opossums, contains .20 species (Gardner 2007). Although its

taxonomy likely will be altered in the future, the choice of the

samples used here increases the chances of dealing with a

single taxonomic unit (particularly for such widely distributed

species as M. domestica). Marked sexual dimorphism is

frequently cited for Monodelphis spp. (Bergallo and Cerqueira

1994; Pine et al. 1985; Ventura et al. 1998). Among the 8

species I sampled, significant SSD was present in M.

brevicaudata, M. domestica, and M. glirina (Table 1),

confirming previous results for the first 2 (Bergallo and

Cerqueira 1994; Ventura et al. 1998), and M. domestica also

presented significant SShD. I could not confirm dimorphism

in M. dimidiata because I had only 1 female specimen.

However, males were larger than the single female in all

views. Based on the observation of sexual dimorphism in M.

dimidiata, Pine et al. (1985) stated that marsupials should be

regarded as extremely dimorphic. However, this study

illustrates that sexual dimorphism is not homogeneous in the

Didelphidae.

Sexual dimorphism in shrew opossums and in the monito

del monte.—This study presents the 1st comprehensive and

comparable assessment of SSD and SShD for most species in

Caenolestidae. Three species presented SSD and SShD in at

least 1 view, particularly Caenolestes fuliginosus and Lestoros

inca (Tables 2 and 3). Previous appraisals of SSD or SShD in

caenolestids are scarce. Bublitz (1987) evaluated sexual

dimorphism in Caenolestidae but reported mainly qualitative

differences between sexes. Albuja and Patterson (1996) report

measurements that suggest sexual dimorphism from species of

Caenolestes but did not provide a statistical analysis of the

data. The lack of sexual dimorphism I found in Dromiciops

gliroides (Microbiotheriidae) confirms previous comments by

Hershkovitz (1999), who stated that living microbiotheriids

were not dimorphic.

Possible sources of sexual dimorphism in New World

opossums.—Sexual dimorphism is usually explained by sexual

selection or as a strategy to avoid niche overlap between sexes

(Shine 1989). Assessing the influence of these factors on

sexual dimorphism in New World marsupials requires

information on social structure, interactions, and precise

ecological niche measurements, all of which are scarce for

the vast majority of species.

In Didelphidae sexual dimorphism increases after sexual

maturity, and it is possibly related to females interrupting growth

by transferring growth-allocated energy to pregnancy and

lactation (Bergallo and Cerqueira 1994; Gardner 1973). Such

an increase in sexual dimorphism also would allow the use of a

wider niche (Cerqueira 1984) and support resource partitioning

(Leite et al. 1994; Pine et al. 1985), but the link between

dimorphism and resource partitioning remains to be tested

properly. I used only adult specimens (i.e., specimens with full

dentition) to avoid influence of ontogenetic differences between

sexes, but recent analyses have shown that sexual maturity occurs

much earlier than the full eruption of all molars and premolars in

several didelphids (Astua and Geise 2006; Dıaz and Flores 2008).

Not only do individuals grow after sexual maturity, but they also

may continue to grow after full eruption of the cheek teeth, thus

possibly further confounding estimates of SSD.

In several Australian marsupials strong SSD also is related

to semelparity (Tyndale-Biscoe and Renfree 1986), where

FIG. 3.—Regressions of sexual size dimorphism (SSD) and sexual shape dimorphism (SShD) on centroid size (CS), using phylogenetic

independent contrasts (PICs), for those views where a significant negative relation was found: A) skull, ventral view, SSD; B) skull, dorsal view,

SShD; C) skull, ventral view, SShD. Both upper bounds (UB) and lower bounds (LB) on degrees of freedom (d.f.) and respective P-values are

presented, according to Purvis and Garland (1993). TD 5 tangent distances. See text for additional details.


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success in agonistic encounters with other males is particularly

important. This is also the proposed reason for the strong

dimorphism and aggressive behavior found in Monodelphis

dimidiata (Gonzalez and Claramunt 2000; Pine et al. 1985).

Gracilinanus agilis and Marmosops paulensis recently have

been reported to be at least partially semelparous (Leiner et al.

2008; Martins et al. 2006a), and both are dimorphic in size and

shape (Tables 2 and 3). So far, semelparity has been reported

only in small-bodied species. Because other taxa with similar

levels of SSD still lack reproductive data, the relation between

body size, semelparity, and dimorphism awaits investigation.

Examination of the scarce available data on social interactions

in New World marsupials suggests that these are apparently

rudimentary, limited mostly to mating and parental care or to

simple agonistic encounters (Charles-Dominique 1983). This

complicates the establishment of a relationship between sexual

dimorphism and social interactions that has been recognized

for other mammals (Lindenfors and Tullberg 1998).

The results presented here do not agree with all previous

estimates of sexual dimorphism. A precise comparison of

these results with previous analyses is hindered by the use of

traditional morphometrics to derive all previous estimates,

thus confounding effects of size and shape. Another possible

source for these differences would be the existence of

geographical variation in sexual dimorphism, as proposed by

Ventura et al. (2002) and empirically confirmed in Caluromys

philander and Metachirus nudicaudatus (Caramaschi 2005;

Silva 2005; Vieira 2006). Contrasting estimates of dimor-

phism in some species of Didelphis (see above) also could be

due to geographic variation. Considering that this is one of the

most abundant genera in collections, this pattern should be

investigated more thoroughly.

Absence of Rensch’s rule within Didelphidae.—Based on a

phylogenetic analysis of 21 taxa, Abouheif and Fairbairn

(1997) concluded that Rensch’s rule is widespread and

general. Explanations for the general occurrence of Rensch’s

rule include a variety of hypotheses that can be summarized as

evolutionary constraints, natural selection, or sexual selection

(Abouheif and Fairbairn 1997; Dale et al. 2007; Serrano-

Meneses et al. 2008). Sexual selection provides the best

explanation of Rensch’s rule in groups such as shorebirds

(Szekely et al. 2004), hummingbirds and flower mites

(Colwell 2000), Aves as a whole (Dale et al. 2007), primates

(Lindenfors and Tullberg 1998), and odonates (Serrano-

Meneses et al. 2008). For all of these taxa natural history,

ecology, and mating systems are sufficiently known from

large, species-rich data sets. Unfortunately, the same is not

true for the vast majority of didelphids. Knowledge of

population ecology and basic behavior are limited, and

possible explanations for the presence or absence of Rensch’s

rule for the majority of these taxa can only be speculative.

The lack of a significant trend in SSD and SShD in relation

to size among didelphids reflects something that can be

observed qualitatively: small-, medium-, and large-bodied

species exist, and in all of these size classes we find some

species that are dimorphic and others with no significant SSD

or SShD. Sexual selection is presumed to have a major

influence in taxa with polygynous mating systems, where it

may lead to selection for larger males. Social structure is

poorly known for most marsupial species, and existing data

refer to a particular community only (Charles-Dominique

1983). Based on available home range data, didelphids appear

to have a promiscuous social system in which males have

overlapping territories and females tend to be more territorial.

Consequently, didelphid males probably do not compete

directly for territories, releasing them from the selective

pressure for increasing body size. This appears to occur in

small-bodied (e.g., Marmosa murina), medium-bodied (e.g.,

Micoureus paraguayanus), and large-bodied (Didelphis and

Philander) species (Caceres 2006; Charles-Dominique 1983).

Apart from mating periods and preweaning periods (when the

young are attached to the mother), didelphids are usually

solitary and do not engage in the formation of structured social

bonds (Charles-Dominique 1983). Thus, examination of the

available data on social interactions and space use in

didelphids does not suggest situations that would lead to

increasing SSD in larger species due to sexual selection.

Contrary to the predictions of Rensch’s rule, I found a

significant negative relationship between sexual dimorphism

and body size in 3 of 5 cases tested. In these cases smaller

species are more dimorphic than larger species, with males

larger than females. A possible explanation could reside in the

reproductive strategy of several smaller species. Over 2

decades ago the highly dimorphic species Monodelphis

dimidiata was suggested to be semelparous (Pine et al.

1985), which would explain its highly aggressive behavior in

male–male encounters (Gonzalez and Claramunt 2000).

Subsequently, based on age classes of museum specimens,

Lorini et al. (1994) proposed that Marmosops incanus also is

semelparous. More recently, detailed population studies have

indicated that Marmosops paulensis and Gracilinanus agilis

exhibit semelparity or partial semelparity (Leiner et al. 2008;

Martins et al. 2006a). In contrast, no records of semelparity are

found for well-studied, large-bodied species, because these

survive for .1 year and reproduce more than once (Tyndale-

Biscoe and Renfree 1986).

Semelparity is associated with strong, male-biased sexual

dimorphism in the well-studied Australian dasyurid marsupi-

als of the genus Antechinus (Fisher and Cockburn 2006;

Kraaijeveld-Smit et al. 2003). Likewise, each of the 4

didelphid species in which semelparity or partial semelparity

has been hypothesized present strong SSD and SShD. In

Antechinus male-biased sexual dimorphism in semelparous

species appears to be driven by sexual selection. Examination

of behavioral and paternity data has shown that larger males

are dominant, more successful in competing for females,

preferred by females, and survive longer than smaller males

(Fisher and Cockburn 2006). Larger males also obtain longer

copulations, produce more sperm, and fertilize a larger

number of females and produce more offspring than smaller

males (Holleley et al. 2006; Kraaijeveld-Smit et al. 2003).

Although no similar data are available for neotropical species,


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a similar process may be acting on small, semelparous

didelphid marsupials.

Reproductive patterns are unknown for most short-tailed

and mouse opossums, but many of these small-bodied genera

have significant SSD or SShD, or both. This presents the

possibility that they share social or reproductive patterns that

favor male-biased SSD. Larger didelphid species tend to

survive longer thus potentially reducing the strength of sexual

selection and leading to less-marked SSD. If this is true, it

could help to explain the occurrence of the inverse of Rensch’s

rule observed in the Didelphidae.

RESUMO

Este estudo avaliou a ocorrencia de dimorfismo sexual de

tamanho (DST) e dimorfismo sexual de forma (DSF) no cranio

e na mandıbula de representantes da maioria das especies das

tres ordens de marsupiais do Novo Mundo, Didelphimorphia,

Paucituberculata e Microbiotheria, atraves de morfometria

geometrica. Tamanhos de centroide e deformacoes parciais

foram extraıdos de marcos anatomicos colocados em imagens

das vistas dorsal, lateral e ventral do cranio e lateral da

mandıbula, e foram comparados entre os sexos para estimar o

DST e DSF. Foram analisados 2932 especimes de 71 especies

de Didelphidae, 5 especies de Caenolestidae e 1 de Micro-

biotheriidae. O DST foi variavel em Didelphimorphia e em

Paucituberculata, e ausente em Microbiotheria. O DSF seguiu

padroes similares, mas o DST e DSF nao estao claramente

acoplados. Tambem foi avaliada a validade da regra de

Rensch—o fenomeno amplamente observado de aumento do

dimorfismo sexual correlacionado com um aumento do

tamanho corporal, quando machos sao maiores que femeas,

ou com uma diminuicao do tamanho corporal, quando femeas

sao maiores que machos—em Didelphidae. Os didelfıdeos

variam em ate duas ordens de grandeza nos seus tamanhos

corporais, e quando existe dimorfismo, machos sao maiores

que femeas. Regressoes dos indicadores de DST e DSF sobre

o tamanho, usando contrastes filogeneticos independente,

indicaram ausencia de relacao significativa entre DST ou DSF

com o aumento do tamanho corporal em nenhuma das

estruturas e vistas analisadas, ou um padrao contrario a regra

de Rensch (especies menores com mais dimorfismo, apesar de

machos serem maiores). Explicacoes para a falta de aderencia

a regra de Rensch em Didelphimorphia podem estar

relacionadas a falta de interacoes sociais ou de territorialidade

em machos, geralmente associadas a este padrao atraves de

selecao sexual. Caso o padrao inverso a regra de Rensch seja

real, uma explicacao pode estar na quantidade crescente de

especies de pequeno tamanho corporal que recentemente

foram descritas como semelparas e portanto sujeitas a uma

selecao mais forte por machos maiores.

ACKNOWLEDGMENTS

I am grateful to the following institutions and professionals

(curators and collection managers) for access to collections under

their care, help during my visits, and sending additional information:

R. Voss (American Museum of Natural History); C. Conroy

(Museum of Vertebrate Zoology, University of California, Berkeley);

J. Salazar-Bravo and W. Gannon (Museum of Southwestern Biology,

University of New Mexico); J. Braun and M. Revelez (Sam Noble

Oklahoma Museum of Natural History); R. Timm (Museum of

Natural History, University of Kansas); B. Patterson and M.

Schulenberg (Field Museum of Natural History); J. Kirsch and P.

Holahan (University of Wisconsin Zoological Museum); A. Gardner,

L. Gordon and C. Ludwig (National Museum of Natural History); L.

Costa, Y. Leite and B. Andrade (Universidade Federal de Minas

Gerais); J. A. Oliveira, L. F. Oliveira, L. Salles and S. Franco (Museu

Nacional, Unversidade Federal do Rio de Janeiro); M. de Vivo and J.

Barros (Museu de Zoologia da Universidade de Sao Paulo); L. Geise

(Universidade do Estado do Rio de Janiero); R. Cerqueira

(Universidade Federal do Rio de Janeiro); and V. Pacheco and E.

Vivar Pinares (Museo de Historia Natural de la Universidad Nacional

de San Marcos). R. Voss also granted me access to material he

personally was studying, including rare specimens. For loans of

several important specimens I am indebted to A. Brunet (James Ford

Bell Museum of Natural History), M. Hafner (Louisiana State

University, Museum of Natural Science), and P. C. A. Simoes-Lopes

and M. Graipel (Universidade Federal de Santa Catarina). I am

grateful to R. Voss and B. Patterson for information on dentition and

morphology of Caenolestidae, D. Flores and S. Solari for help in

determining Thylamys species, and M. Guenther, E. Dumont, and an

anonymous reviewer for several revisions and suggestions that

improved the clarity and quality of this manuscript. The author was

supported throughout this project by a doctoral fellowship from

Fundacao de Amparo a Pesquisa do Estado de Sao Paulo, (00/11444-

7), and a Grant-in-Aid of Research from the American Society of

Mammalogists. This work is presently supported by a grant from

Fundacao de Amparo a Ciencia e Tecnologia do Estado de

Pernambuco (APQ-0351-2.04/06).

LITERATURE CITED

ABOUHEIF, E., AND D. J. FAIRBAIRN. 1997. A comparative analysis of

allometry for sexual size dimorphism: assessing Rensch’s rule.

American Naturalist 149:540–562.

ALBUJA, L., AND B. D. PATTERSON. 1996. A new species of northern

shrew-opossum (Paucituberculata: Caenolestidae) from the Cor-

dillera del Condor, Ecuador. Journal of Mammalogy 77:41.

ALONSO-MEJIA, A., AND R. A. MEDELLIN. 1992. Marmosa mexicana.

Mammalian Species 421:1–4.

ASTUA, D., AND L. GEISE. 2006. Early reproductive onset in the white-

eared opossum, Didelphis albiventris Lund, 1840 (Didelphimor-

phia, Didelphidae). Mammalian Biology 71:299–303.

ASTUA, D., AND N. O. LEINER. 2008. Tooth eruption sequence and

replacement pattern in woolly opossums, genus Caluromys

(Didelphimorphia: Didelphidae). Journal of Mammalogy 89:244–

251.

ASTUA DE MORAES, D. 2004. Evolucao morfologica do cranio e

elementos pos-cranianos dos marsupiais americanos (Didelphi-

morphia, Paucituberculata, Microbiotheria). Ph.D. dissertation,

Universidade de Sao Paulo, Sao Paulo, Brasil.

ASTUA DE MORAES, D., E. HINGST-ZAHER, L. F. MARCUS, AND R.

CERQUEIRA. 2000. A geometric morphometric analysis of cranial

and mandibular shape variation of didelphid marsupials. Hystrix,

Italian Journal of Mammalogy, New Series 11:115–130.

BERGALLO, H. G., AND R. CERQUEIRA. 1994. Reproduction and growth

of the opossum Monodelphis domestica (Mammalia, Didelphidae)

in northeastern Brazil. Journal of Zoology (London) 232:551–563.


Dow


ic.oup.com/jm

amm


BUBLITZ, J. 1987. Untersuchungen zur Systematik der rezenten

Caenolestidae Trouessart, 1898: unter Verwendung craniomea-

trischer Methoden. Bonner Zoologische Monographien 23:1–96.

CACERES, N. C. 2006. Uso do espaco por marsupiais: fatores

influentes, comportamento e heterogeneidade espacial. Pp. 203–

215 in Os marsupiais do Brasil: biologia, ecologia e evolucao (N.

C. Caceres and E. L. A. Monteiro-Filho, eds.). Editora da

Universidade Federal do Mato Grosso do Sul, Campo Grande,

Brasil.

CARAMASCHI, F. P. 2005. Variacao geografica em Caluromys

philander (Linnaeus, 1758) no Brasil (Didelphimorphia: Didelphi-

dae). M.S. thesis, Museu Nacional/Universidade Federal do Rio de

Janeiro, Rio de Janeiro, Brasil.

CARDILLO, M., O. R. P. BININDA-EMONDS, E. BOAKES, AND A. PURVIS.

2004. A species-level phylogenetic supertree of marsupials.

Journal of Zoology (London) 264:11–31.

CARDINI, A., AND P. TONGIORGI. 2003. Yellow-bellied marmots

(Marmota flaviventris) ‘in the shape space’ (Rodentia, Sciuridae):

sexual dimorphism, growth and allometry of the mandible.

Zoomorphology 122:11–23.

CARMIGNOTTO, A. P., AND T. MONFORT. 2006. Taxonomy and

distribution of the Brazilian species of Thylamys (Didelphimor-

phia: Didelphidae). Mammalia 70:126–144.

CERQUEIRA, R. 1984. Reproduction de Didelphis albiventris dans le

nord-est du Bresil (Polyprotodontia, Didelphidae). Mammalia

48:95–104.

CERQUEIRA, R., AND B. LEMOS. 2000. Morphometric differentiation

between neotropical black-eared opossums, Didelphis marsupialis

and D. aurita (Didelphimorphia, Didelphidae). Mammalia 64:319–

327.

CHARLES-DOMINIQUE, P. 1983. Ecology and social adaptations in

didelphid marsupials: comparison with eutherians of similar

ecology. Pp. 341–435 in Advances in the study of mammalian

behavior (J. F. Eisenberg and D. G. Kleiman, eds.). Special

Publication 7, The American Society of Mammalogists.

COLWELL, R. K. 2000. Rensch’s rule crosses the line: convergent

allometry of sexual size dimorphism in hummingbirds and flower

mites. American Naturalist 156:495–510.

COSTA, L. P., Y. L. R. LEITE, AND J. L. PATTON. 2003. Phylogeography

and systematic notes on two species of gracile mouse opossums,

genus Gracilinanus (Marsupialia: Didelphidae) from Brazil.

Proceedings of the Biological Society of Washington 116:275–

292.

DALE, J., P. O. DUNN, J. FIGUEROLA, T. LISLEVAND, T. SZEKELY, AND L.

A. WHITTINGHAM. 2007. Sexual selection explains Rensch’s rule of

allometry for sexual size dimorphism. Proceedings of the Royal

Society of London, B. Biological Sciences 274:2971–2979.

DIAZ, M. M., AND D. A. FLORES. 2008. Early reproduction onset in

four species of Didelphimorphia in the Peruvian Amazonia.

Mammalia 72:126–130.

DROVETSKI, S. V., S. ROHWER, AND N. A. MODE. 2006. Role of sexual

and natural selection in evolution of body size and shape: a

phylogenetic study of morphological radiation in grouse. Journal of

Evolutionary Biology 19:1083–1091.

FALCONER, D. S. 1989. Introduction to quantitative genetics. Long-

man, Essex, United Kingdom.

FELSENSTEIN, J. 1985. Phylogenies and the comparative method.


FISHER, D. O., AND A. COCKBURN. 2006. The large-male advantage in

brown antechinuses: female choice, male dominance, and delayed

male death. Behavioral Ecology 17:164–171.

FRANKLIN, D., L. FREEDMAN, N. MILNE, AND C. E. OXNARD. 2006. A

geometric morphometric study of sexual dimorphism in the crania

of indigenous southern Africans. South African Journal of Science

102:229–238.

GARDNER, A. L. 1973. The systematics of the genus Didelphis

(Marsupialia: Didelphidae) in North and Middle America. Special

Publications, The Museum, Texas Tech University 4:4–81.

GARDNER, A. L. 2007. Mammals of South America. University of

Chicago Press, Chicago, Illinois.

GARLAND, T., AND R. DIAZ-URIARTE. 1999. Polytomies and

phylogenetically independent contrasts: examination of the

bounded degrees of freedom approach. Systematic Biology

48:547–558.

GIDASZEWSKI, N. A., M. BAYLAC, AND C. P. KLINGENBERG. 2009.

Evolution of sexual dimorphism of wing shape in the Drosophila

melanogaster subgroup. BMC Evolutionary Biology 9:110.

GONZALEZ, E. M., AND S. CLARAMUNT. 2000. Behaviors of captive

short-tailed opossums, Monodelphis dimidiata (Wagner, 1847)

(Didelphimorphia, Didelphidae). Mammalia 64:271–285.

GRAIPEL, M., P. R. M. MILLER, AND A. XIMENEZ. 1996. Contribuicao a

identificacao e distribuicao das subespecies de Lutreolina crassi-

caudata (Desmarest) (Marsupialia, Didelphidae). Revista Brasi-

leira de Zoologia 13:781–790.

HARVEY, P. H., AND M. D. PAGEL. 1991. The comparative method in

evolutionary biology. Oxford University Press, Oxford, United

Kingdom.

HERSHKOVITZ, P. 1999. Dromiciops gliroides Thomas, 1894, last of the

Microbiotheria (Marsupialia), with a review of the family

Microbiotheriidae. Fieldiana: Zoology (New Series) 93:1–60.

HOLLELEY, C. E., C. R. DICKMAN, M. S. CROWTHER, AND B. P.

OLDROYD. 2006. Size breeds success: multiple paternity, multivar-

iate selection and male semelparity in a small marsupial,

Antechinus stuartii. Molecular Ecology 15:3439–3448.

HOOD, C. S. 2000. Geometric morphometric approaches to the study

of sexual size dimorphism in mammals. Hystrix, Italian Journal of

Mammalogy, New Series 11:77–89.

JANSA, S. A., AND R. VOSS. 2005. Phylogenetic relationships of the

marsupial genus Hyladelphys based on nuclear gene sequences and

morphology. Journal of Mammalogy 86:853–865.

KRAAIJEVELD-SMIT, F. J. L., S. J. WARD, AND P. D. TEMPLE-SMITH.

2003. Paternity success and the direction of sexual selection in a

field population of a semelparous marsupial, Antechinus agilis.

Molecular Ecology 12:475–484.

LEINER, N. O., E. Z. F. SETZ, AND W. R. SILVA. 2008. Semelparity and

factors affecting the reproductive activity of the Brazilian slender

opossum (Marmosops paulensis) in southeastern Brazil. Journal of

Mammalogy 89:153–158.

LEITE, Y. L. R., J. R. STALLINGS, AND L. P. COSTA. 1994. Particao de

recursos entre especies simpatricas de marsupiais na Reserva

Biologica de Poco das Antas, Rio de Janeiro. Revista Brasileira de

Biologia 54:525–536.

LEMOS, B., AND R. CERQUEIRA. 2002. Morphological differentiation in

the white-eared opossum group (Didelphidae: Didelphis). Journal

of Mammalogy 83:354–369.

LEMOS, B., G. MARROIG, AND R. CERQUEIRA. 2001. Evolutionary rates

and stabilizing selection in large-bodied opossum skulls (Didel-

phimorphia: Didelphidae). Journal of Zoology (London) 255:181–

189.

LINDENFORS, P., AND B. S. TULLBERG. 1998. Phylogenetic analyses of

primate size evolution: the consequences of sexual selection.

Biological Journal of the Linnean Society 64:413–447.


Dow


ic.oup.com/jm

amm


LOPEZ-FUSTER, M. J., R. PEREZ-HERNANDEZ, J. VENTURA, AND M.

SALAZAR. 2000. Effect of environment on skull-size variation in

Marmosa robinsoni in Venezuela. Journal of Mammalogy 81:829.

LOPEZ-FUSTER, M. J., M. SALAZAR, R. PEREZ-HERNANDEZ, AND J.

VENTURA. 2002. Craniometrics of the orange mouse opossum

Marmosa xerophila (Didelphimorphia: Didelphidae) in Venezuela.

Acta Theriologica 47:201–209.

LORINI, M. L., J. A. OLIVEIRA, AND V. G. PERSSON. 1994. Annual age

structure and reproductive patterns in Marmosa incana (Lund,

1841) (Didelphidae, Marsupialia). Zeitschrift fur Saugetierkunde

59:65–73.

LUCKETT, W. P., AND N. HONG. 2000. Ontogenetic evidence for dental

homologies and premolar replacement in fossil and extant

Caenolestids (Marsupialia). Journal of Mammalian Evolution

7:109–127.

LUNDE, D. P., AND W. A. SCHUTT. 1999. The peculiar carpal tubercles

of male Marmosops parvidens and Marmosa robinsoni (Didelphi-

dae: Didelphinae). Mammalia 63:495–504.

MADDISON, W. P., AND D. R. MADDISON. 2008. Mesquite: a modular

system for evolutionary analysis. Version 2.5. http://mesquiteproject.

org. Accessed 9 June 2008.

MARTINS, E. G., V. BONATO, C. Q. DA-SILVA, AND S. R. F. DOS REIS.

2006a. Partial semelparity in the neotropical didelphid marsupial

Gracilinanus microtarsus. Journal of Mammalogy 87:915–920.

MARTINS, E. G., V. BONATO, H. P. PINHEIRO, AND S. F. DOS REIS. 2006b.

Diet of the gracile mouse opossum (Gracilinanus microtarsus)

(Didelphimorphia: Didelphidae) in a Brazilian cerrado: patterns of

food consumption and intrapopulation variation. Journal of

Zoology (London) 269:21–28.

MARTINS, E. P., AND T. F. HANSEN. 1997. Phylogenies and the

comparative method: a general approach to incorporating phylo-

genetic information into the analysis of interspecific data.


MAUNZ, M., AND R. Z. GERMAN. 1996. Craniofacial heterochrony and

sexual dimorphism in the short-tailed opossum (Monodelphis

domestica). Journal of Mammalogy 77:992.

MIDFORD, P. E., T. GARLAND, JR., AND W. P. MADDISON. 2008.

PDAP:PDTREE package for Mesquite, version 1.13. http://

mesquiteproject.org. Accessed 30 July 2008.

MONTEIRO-FILHO, E. L. A., L. R. MONTEIRO, AND S. F. REIS. 2002. Skull

shape and size divergence in dolphins of the genus Sotalia: a tridimen-

sional morphometric analysis. Journal of Mammalogy 83:125–134.

O’HIGGINS, P., AND M. COLLARD. 2004. Sexual dimorphism and facial

growth in papionin monkeys. Journal of Zoology (London)

257:255–272.

O’CONNELL, M. A. 1983. Marmosa robinsoni. Mammalian Species

203:1–6.

OLIVEIRA, J. A., M. L. LORINI, AND V. G. PERSSON. 1992. Pelage

variation in Marmosa incana (Didelphidae, Marsupialia) with

notes on taxonomy. Zeitschrift fur Saugetierkunde 57:129–136.

PAGEL, M. D. 1992. A method for the analysis of comparative data.

Journal of Theoretical Biology 156:431–442.

PATTON, J. L., AND L. P. COSTA. 2003. Molecular phylogeography and

species limits in rainforest didelphid marsupials of South America.

Pp. 63–81 in Predators with pouches: the biology of carnivorous

marsupials (M. E. Jones, C. R. Dickman, and M. Archer, eds.).

CSIRO Publishing, Collingwood, Australia.

PATTON, J. L., M. N. F. DA SILVA, AND J. R. MALCOLM. 2000. Mammals

of the Rio Jurua and the evolutionary and ecological diversification

of Amazonia. Bulletin of the American Museum of Natural History

244:1–306.

PINE, R. H. 1981. Reviews of the mouse opossums Marmosa parvidens

Tate and Marmosa invicta Goldman (Mammalia: Marsupialia:

Didelphidae) with description of a new species. Mammalia 45:55–70.

PINE, R. H., P. L. DALBY, AND J. O. MATSON. 1985. Ecology, postnatal

development, morphometrics, and taxonomic status of the short-

tailed opossum, Monodelphis dimidiata, an apparently semelparous

annual marsupial. Annals of Carnegie Museum 54:195–231.

PURVIS, A., AND T. GARLAND, JR. 1993. Polytomies in comparative

analyses of continuous data. Systematic Biology 42:569–575.

RICHARD-HANSEN, C., J. C. VIE, N. VIDAL, AND J. KERAVEC. 1999. Body

measurements on 40 species of mammals from French Guiana.

Journal of Zoology (London) 247:419.

ROHLF, F. J. 2006. TPSDig. Available from the author at Department

of Ecology and Evolution, State University of New York at Stony

Brook, Stony Brook.

ROHLF, F. J., AND D. SLICE. 1990. Extensions of the Procrustes method

for the optimal superimposition of landmarks. Systematic Zoology

39:40–59.

ROSSI, R. V. 2005. Revisao taxonomica de Marmosa Gray, 1821

(Didelphimorphia: Didelphidae). Ph.D. dissertation, Universidade

de Sao Paulo, Sao Paulo, Brasil.

SERRANO-MENESES, M. A., A. CORDOBA-AGUILAR, M. AZPILICUETA-

AMORIN, E. GONZALEZ-SORIANO, AND T. SZEKELY. 2008. Sexual

selection, sexual size dimorphism and Rensch’s rule in Odonata.

Journal of Evolutionary Biology 21:1259–1273.

SHEETS, H. D. 2004. IMP suite—integrated morphometrics package.

http://www.canisius.edu/,sheets/morphsoft.html. Accessed 5 Au-

gust 2004.

SHINE, R. 1989. Ecological causes for the evolution of sexual

dimorphism: a review of the evidence. Quarterly Review of

Biology 64:419–461.

SILVA, H. S. 2005. Variacao geografica em Metachirus nudicaudatus

(Didelphimorphia, Didelphidae) na Mata Atlantica. M.S. thesis,

Museu Nacional/Universidade Federal do Rio de Janeiro, Rio de

Janeiro, Brasil.

SMITH, F. A., ET AL. 2003. Body mass of late Quaternary mammals.

Ecology 84:3403.

SMITH, R. J. 1999. Statistics of sexual size dimorphism. Journal of

Human Evolution 36:423–459.

SMITH, R. J., AND J. M. CHEVERUD. 2002. Scaling of sexual

dimorphism in body mass: a phylogenetic analysis of Rensch’s

rule in primates. International Journal of Primatology 23:1098–

1135.

SOLARI, S. 2003. Diversity and distribution of Thylamys (Didelphi-

dae) in South America, with emphasis on species from the

western side of the Andes. Pp. 82–101 in Predators with pouches:

the biology of carnivorous marsupials (M. E. Jones, C. R.

Dickman, and M. Archer, eds.). CSIRO Publishing, Collingwood,

Australia.

STEINER, C., AND F. M. CATZEFLIS. 2003. Mitochondrial diversity and

morphological variation of Marmosa murina (Didelphidae) in

French Guiana. Journal of Mammalogy 84:822.

SZEKELY, T., R. P. FRECKLETON, AND J. D. REYNOLDS. 2004. Sexual

selection explains Rensch’s rule of size dimorphism in shorebirds.

Proceedings of the National Academy of Sciences 101:12224–

12227.

TRIBE, C. J. 1990. Dental age classes in Marmosa incana and other

didelphoids. Journal of Mammalogy 71:566–569.

TYNDALE-BISCOE, C. H., AND R. B. MACKENZIE. 1976. Reproduction in

Didelphis marsupialis and D. albiventris in Colombia. Journal of

Mammalogy 57:249–265.


Dow


ic.oup.com/jm

amm


TYNDALE-BISCOE, C. H., AND M. B. RENFREE. 1986. Reproductive

physiology of marsupials. Cambridge University Press, Cam-

bridge, United Kingdom.

VENTURA, J., R. PEREZ-HERNANDEZ, AND M. J. LOPEZ-FUSTER. 1998.

Morphometric assessment of the Monodelphis brevicaudata group

(Didelphimorphia: Didelphidae) in Venezuela. Journal of Mam-

malogy 79:104.

VENTURA, J., M. SALAZAR, R. PEREZ-HERNANDEZ, AND M. J. LOPEZ-

FUSTER. 2002. Morphometrics of the genus Didelphis (Didelphi-

morphia: Didelphidae) in Venezuela. Journal of Mammalogy

83:1087.

VIEIRA, C.L.G.C. 2006. Sistematica do jupati Metachirus Burmeister,

1854 (Mammalia: Didelphimorphia). M.S. thesis, Universidade

Federal do Espirito Santo, Vitoria, Brasil.

VOSS, R. S., AND S. A. JANSA. 2003. Phylogenetic studies on didelphid

marsupials II. Nonmolecular data and new IRBP sequences:

separate and combined analyses of didelphine relationships with

denser taxon sampling. Bulletin of the American Museum of

Natural History 276:1–82.

VOSS, R. S., AND S. A. JANSA. 2009. Phylogenetic relationships and

classification of didelphid marsupials, an extant radiation of New

World metatherian mammals. Bulletin of the American Museum of


VOSS, R. S., D. P. LUNDE, AND S. JANSA. 2005. On the contents

of Gracilinanus Gardner and Creighton, 1989, with the

description of a previously unrecognized clade of small

didelphid marsupials. American Museum Novitates 3482:

1–34.

VOSS, R. S., D. P. LUNDE, AND N. B. SIMMONS. 2001. The mammals of

Paracou, French Guiana: a neotropical lowland rainforest fauna—

part 2. Nonvolant species. Bulletin of the American Museum of


VOSS, R. S., T. TARIFA, AND E. YENSEN. 2004. An introduction to

Marmosops (Marsupialia: Didelphidae), with the description of a

new species from Bolivia and notes on the taxonomy and distribution

of other Bolivian forms. American Museum Novitates 3466:1–40.

ZAR, J. H. 1996. Biostatistical analysis. 3rd ed. Prentice Hall, Inc.,

Upper Saddle River, New Jersey.

ZELDITCH, M. L., D. L. SWIDERSKI, H. D. SHEETS, AND W. L. FINK. 2004.

Geometric morphometrics for biologists: a primer. Elsevier

Academic Press, Boston, Massachusetts.

Submitted 14 January 2009. Accepted 25 January 2010.

Associate Editor was Elizabeth R. Dumont.


Dow


ic.oup.com/jm

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